Research progress on sugar metabolism and concentration regulation in fruit

Abstract: Soluble sugars, including sucrose, fructose and glucose, are not only essential to fleshy fruit growth and development but also central to fruit quality. Fruit taste and flavor are positively related to the composition and concentration of sugars. As the composition and concentration of sugars during fruit maturation are determined by metabolic and transport processes during fruit development, under-standing these processes and their regulation is significant for fruit quality improvement. This article fo-cuses on the key role of sugar metabolism-related enzymes and key genes in the regulation of sugar con-tent and the physiological and biochemical processes of sugar signals in response to different environ-mental changes. It aims to provide a theoretical reference for improving fruit quality and increasing yield. At the center of sugar metabolism in sink cells is the sucrose cycle, previously called futile recy-cle, which includes the breakdown of sucrose by invertase and sucrose synthase (SUSY, EC 2.4.1.13), the phosphorylation of the resulting hexoses and the interconversion between hexose phosphates and UDP- glucose (UDPG), and the re- synthesis of sucrose via sucrose- 6- phosphate synthase (SPS, EC2.4.1.14) and sucrose-6-phosphate phosphatase (EC 3.1.3.24). This metabolic system is associated with many other metabolic pathways, such as glycolysis and tricarboxylic acid (TCA) cycle, starch synthesis and cellulose synthesis, and its coordination with the sugar transport system on the tonoplast is expected to determine the distribution of sugars between metabolism in the cytosol and accumulation in the vacu-ole. In apple and other Rosaceae species, sorbitol is an important carbohydrate transported from source tissues through the phloem to the sink, accounting for 60-80% of the total carbon in leaves. In source leaves, sorbitol is synthesized from glucose-6-phosphate (G6P) in a two-step process: G6P is first con-verted to sorbitol-6-phosphate (S6P) via aldose-6-phosphate reductase (A6PR; EC 1.1.1.200), then fol-lowed by dephosphorylation of S6P to sorbitol via S6P phosphatase. The loading of both sorbitol and su-crose into the companion cell-sieve element (SE-CC) complex through a symplastic pathway. After be-ing unloaded from SE-CC complexes into the cell wall space in fruit, sorbitol is taken up into the cyto-sol of parenchyma cells by sorbitol transporter (SOT), and then converted to fructose by sorbitol dehy-drogenase (SDH, EC1.1.1.14). Sucrose is directly transported into parenchyma cells by sucrose trans-porters (SUT), or converted to glucose and fructose by cell wall invertase (CWINV) first, and then transported into parenchyma cells by hexose transporters. Once taken up into parenchyma cells of fruit, both sorbitol and sucrose feed into the sucrose cycle to meet the carbon requirement for fruit growth and development while excess carbon is converted to starch for storage in plastids or transported into vacuole by sugar transporters for accumulation. Transporter-mediated sugar accumulation in the vacu-ole is related to the regulation of sugars available in the cytosol. However, the availability and composi-tion of sugars are highly regulated by sugar metabolism. Photosynthetic products in leaves are transport- ed through protein transmembrane and a series of enzyme reactions and finally disperse in different parts of the fruit in the form of sucrose, fructose and glucose, which endows the fruit with a unique fla-vor quality. Sorbitol metabolism, sucrose metabolism, and hexose metabolism pathway are three major sugar metabolism pathways, in which different types of metabolic enzymes are involved. Currently, ma-jor metabolic enzymes include suc-phosphate synthase (SPS), sucrose synthase (SUSY), neutral inver-tase (NINV) and fructokinase (FRK). In terms of sugar-related metabolic enzyme genes, the expression differences in related metabolic genes in different fruit growth and development periods will lead to dif-ferences in the amount of sugar accumulation. Many sugar-related genes have been cloned through bio-technology from different species, such as SDH1 and FRK2. In fleshy fruits, the concentration and dis-tribution of sugars in parenchyma cells are affected via this cycle by environmental factors, such as wa-ter, light and temperature, respectively. The dynamic changes of sugar components are strictly regulated by key metabolic enzymes and genes, including SUSY, FRK, and some transporters. Thus, more re-search and techniques are needed to understand how to control metabolic enzymes to provide sufficient nutrients for plant growth and development in appropriate time, space and quantity, such as dynamic ra- dioactive tracer imaging technology for phloem transport, dynamic interpretation of sugar transport, me-tabolism, and accumulation under different environmental conditions. Plants are equally faced with chal-lenges brought by fungal diseases, such as powdery mildew and brown spot, especially in fruit trees. Af-ter plants are infected with the pathogen, increasing invertase activity could change the proportion of ex-tracellular hexose/sucrose and cause hexose-mediated defense response. In addition, genome engineer-ing methods can change transcription regulation or protein modification affecting pathogen-targeted in-vertase activity (CWINV) or sugar transporters (SWEET4), and produce resistance to pathogens with-out affecting fruit quality, thus providing essential strategies for plant defense against diseases. There-fore, a comprehensive study on the relationship between environmental factors and fruit sugar content can provide a theoretical basis for the ecological regulation of fruit sugar metabolism and achieve the goal of improving fruit quality through effective environmental regulation measures. Further study on the regulation mechanism of sugar metabolism-related enzymes and key gene expression on fruit sugar content has theoretical and practical significance for fundamentally improving fruit quality.